Thermal sensitivity of field metabolic rate predicts differential futures for bluefin tuna juveniles across the Atlantic Ocean

Changing environmental temperatures impact the physiological performance of fishes, and consequently their distributions. A mechanistic understanding of the linkages between experienced temperature and the physiological response expressed within complex natural environments is often lacking, hampering efforts to project impacts especially when future conditions exceed previous experience. In this study, we use natural chemical tracers to determine the individual experienced temperatures and expressed field metabolic rates of Atlantic bluefin tuna (Thunnus thynnus) during their first year of life. Our findings reveal that the tuna exhibit a preference for temperatures 2–4 °C lower than those that maximise field metabolic rates, thereby avoiding temperatures warm enough to limit metabolic performance. Based on current IPCC projections, our results indicate that historically-important spawning and nursery grounds for bluefin tuna will become thermally limiting due to warming within the next 50 years. However, limiting global warming to below 2 °C would preserve habitat conditions in the Mediterranean Sea for this species. Our approach, which is based on field observations, provides predictions of animal performance and behaviour that are not constrained by laboratory conditions, and can be extended to any marine teleost species for which otoliths are available.


Supplementary text
ABFT ecology / management background Since the mid 1970s Atlantic BFT have been considered as two stocks separated by the 45°W management boundary, the western stock spawning in or near the Gulf of Mexico and potentially the adjacent shelf sea of the eastern US and the larger eastern stock spawning in or near the Mediterranean.The weight of evidence from conventional tagging, biologging, genetic and otolith microchemistry approaches supports this broad assessment although with uncertainty concerning the possibility of additional spawning areas (e.g.Slope Sea [1][2][3] ) the degree and timing of trans-Atlantic migrations and the existence of sub-population structure within the Mediterranean 4 .Consequently, the international Commission for the Conservation of Atlantic Tunas (ICCAT) manages ABFT as two distinct stocks with natal fidelity, but allowing for intermixing of stocks.The importance of climate change impacts from a tuna fishery management perspective has recently been recognised by ICCAT with adoption of the first resolution on climate change.
Eastern and western populations of ABFT show different life history and growth trajectories with western populations typically slower growing.In both populations, spawning occurs in waters warmer than 21 °C4 , and larval tuna are associated with water temperatures from 20-28 °C.Consequently, spawning occurs earlier in the warmer western North Atlantic / Gulf of Mexico (April-June) than in the Mediterranean (May to July, east-west) 5,6 .Eastern ABFT remain in the Mediterranean sea for around a year, typically arriving in fisheries at the Bay of Biscay at a mean size of 60cm.The location and distribution of juvenile western ABFT is less well known 7 , but larval and juvenile tuna in Gulf of Mexico are seldom found where SST exceeds 29°C 8 .Eastern ABFT mature earlier and at smaller body size, with an estimated 50% maturity at 3-8 years and at 130-200 cm, compared to uncertain but estimated > 8 years to reach maturity for western-origin ABFT.Differences in size at maturity between the two populations have been reported; in the western population, maturity is assumed to be achieved in fish no younger than nine years old or 185 cm curved fork length 9 , while in the Mediterranean Sea 100% of ABFT show to be mature at >135 cm fork length (i.e., age 4-5 years) 10 .However, the similarity in growth rates of both components has raised doubts regarding the difference in age of sexual maturity, and novel approaches for assessing sexual maturity in ABFT suggest that maturity ogives for ABFT originated from the western and eastern populations are indeed similar.

Otolith FMR proxy background
Oxygen in otolith aragonite is deposited at, or close to, isotopic equilibrium with the ambient water, with a temperature-dependent fractionation such that the temperature of otolith precipitation can be estimated from knowledge of the isotopic compositions of the ambient water and the otolith.Carbon in otolith aragonite is not in isotopic equilibrium with the surrounding dissolved inorganic carbon [11][12][13] .Rather, carbon in the blood is a mixture of carbon derived from dissolved inorganic carbonate and carbon released from respiration of food.The stable isotope composition of these sources is very different: seawater carbon (d 13 Csw) values typically range between c.1 and -7‰ globally, while respiratory carbon (d 13 Cresp) values generally vary between c. -10 to -25‰ in marine fishes.Otolith carbonate biomineral is formed from a mixture of these sources of HCO3 -ions transported from blood into the biomineralising medium (endolymph fluid within the inner ear sacculus).The isotopic composition of inorganic carbon in blood, the endolymph fluid and otolith aragonite mineral is a weighted average of the relative contribution of respiratory carbon and seawater dissolved carbon 12,[14][15][16][17] .Critically, as the rate of respiration of food sources increases, the relative proportion of respiratory carbon in blood increases.The proportion of respiratory carbon in otolith aragonite (otolith Cresp) can be determined from isotopic mass balance given estimates of the isotopic composition of diet and seawater carbon sources, providing a proxy measure of FMR averaged over the timeframe of otolith growth [18][19][20][21][22][23][24][25] .

Limitations of data
The data analysed in this study were obtained opportunistically with respect to investigating Supp.Fig. S1: Sustained reduction in the proportion of ABFT assigned to a western (Gulf of Mexico) origin seen in adult tuna captured in the East, West and Central regions of the North Atlantic.Year class represents birth year of the fish determined by otolith ageing.Data and code are available thermal sensitivity of physiological performance data.Consequently the data are unbalanced sampling across years, ages and sites of origin.Samples of fish collected as fish older than 2 years of age are influenced by unbalanced collection across years of sampling and assigned juvenile origin.Most fish are assigned to a Mediterranean origin (Supp Fig S1), and consequently few fish experienced temperatures likely to result in thermal limitation.Additionally fish experiencing sub-optimal temps in the first year of life may be less likely to survive to adulthood.Consequently there are relatively few individuals available to constrain thermal performance at temperatures in excess of 28°C.Furthermore, the gulf of Mexico and Mediterranean have different d18 Owater values, but assigned origin for fish caught as adults in central Atlantic is based on otolith d 18 O values, creating a false break in inferred temperatures (Fig.3D).These constraints do not apply to young of the year or yearling data which were sampled specifically in a single year and from known origin individuals to validate juvenile d 18 O values.Consequently, yearling data provide best estimates of the thermal sensitivity of Cresp values.

Table S1 .
List of models and corresponding institutions.

Table S2 .
A Brief description of different future climate scenarios of the CMIP6 projections used in this study.